Determining the bacterial cell biology of Planctomycetes

Boedeker, Christian; Schüler, Margarete; Reintjes, Greta; Jeske, Olga; Teeseling, Muriel C. F. van; Jogler, Mareike; Rast, Patrick; Borchert, D.; Devos, Damien P.; Kucklick, Martin; Schaffer, Miroslava; Kolter, Roberto; Niftrik, Laura van; Engelmann, Susanne; Amann, Rudolf; Rohde, Manfred; Engelhardt, Harald; Jogler, Christian

doi:10.1038/ncomms14853

Cited by 180 publications

(167 citation statements)

References 65 publications

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“…Like the eukaryotic equivalent, DNA replication and transcription occur inside the phage nucleus, while translation and metabolic enzymes are localized in the cytoplasm. While a membrane bound structure containing chromosomal DNA has been reported in Planctomycetes , it also contains ribosomes, indicating that proteins and DNA are not compartmentalized separately (Boedeker et al, 2017; Fuerst and Sagulenko, 2011; Sagulenko et al, 2017). The subcellular organization observed during phage 201Φ2-1 infection of P. chlororaphis is unique, and prompted us to investigate if it is conserved during replication of other phages.…”

Section: Introductionmentioning

confidence: 99%

The Phage Nucleus and Tubulin Spindle Are Conserved among Large Pseudomonas Phages

et al. 2017

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Summary We recently demonstrated that the large Pseudomonas chlororaphis bacteriophage 201φ2-1 assembles a nucleus-like structure that encloses phage DNA and segregates proteins according to function, with DNA processing proteins inside and metabolic enzymes and ribosomes outside the nucleus. Here we investigate the replication pathway of the Pseudomonas aeruginosa bacteriophages φKZ and φPA3. Bacteriophages φKZ and φPA3 encode a proteinaceous shell that assembles a nucleus-like structure that compartmentalizes proteins and DNA during viral infection. We show that the tubulin-like protein PhuZ encoded by each phage assembles a bipolar spindle that displays dynamic instability and positions the nucleus at midcell. Our results suggest that the phage spindle and nucleus play the same functional role in all three phages, 201φ2-1, φKZ and φPA3, demonstrating that these key structures are conserved among large Pseudomonas phages.

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Section: Introductionmentioning

confidence: 99%

The Phage Nucleus and Tubulin Spindle Are Conserved among Large Pseudomonas Phages

et al. 2017

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“…The phylum Planctomycetes comprises ubiquitous bacteria with a usually spherical cell shape that have an ecological relevance in many soil, freshwater and marine environments (Fuerst and Sagulenko, 2011;Boedeker et al, 2017). Taxonomically this phylum is currently divided into the two classes Planctomycetia and Phycisphaerae.…”

Section: Introductionmentioning

confidence: 99%

Genome biology of a novel lineage of planctomycetes widespread in anoxic aquatic environments

Spring

Bunk

Spröer

et al. 2018

Environmental Microbiology

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Anaerobic strains affiliated with a novel order-level lineage of the Phycisphaerae class were retrieved from the suboxic zone of a hypersaline cyanobacterial mat and anoxic sediments of solar salterns. Genome sequences of five isolates were obtained and compared with metagenome-assembled genomes representing related uncultured bacteria from various anoxic aquatic environments. Gene content surveys suggest a strictly fermentative saccharolytic metabolism for members of this lineage, which could be confirmed by the phenotypic characterization of isolates. Genetic analyses indicate that the retrieved isolates do not have a canonical origin of DNA replication, but initiate chromosome replication at alternative sites possibly leading to an accelerated evolution. Further potential factors driving evolution and speciation within this clade include genome reduction by metabolic specialization and rearrangements of the genome by mobile genetic elements, which have a high prevalence in strains from hypersaline sediments and mats. Based on genetic and phenotypic data a distinct group of strictly anaerobic heterotrophic planctomycetes within the Phycisphaerae class could be assigned to a novel order that is represented by the proposed genus Sedimentisphaera gen. nov. comprising two novel species, S. salicampi gen. nov., sp. nov. and S. cyanobacteriorum gen. nov., sp. nov.

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“…In contrast, a unique cell plan provides a distinct way for free-living Planctomycetes to obtain scarce resource (Wiegand et al 2018). The results of the latest comprehensive studies indicate the existence of an exceptionally enlarged periplasmic space in planctomycetal cells (Boedeker et al 2017), where entire high-molecular weight polysaccharides can be transported into their enlarged periplasm. This strategy would allow for the slow degradation of diverse and complex substrates in the sheltered environment of the periplasmic space without the need to secret a plethora of different enzymes.…”

Section: Discussionmentioning

confidence: 99%

Stratification of microbiomes during the holomictic period of Lake Fuxian, an alpine monomictic lake

Xing

Tao

Luo

et al. 2019

Limnology & Oceanography

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In warm monomictic lakes, the hypolimnion is important for accumulating and decomposing organic matter derived from surface production, and the regenerated nutrients will be supplied to the epilimnion through winter vertical mixing. So far, we know little about microbial community composition and function in the hypolimnion when the significant thermal stratification disappears. In this study, we investigated microbial community compositions and functional gene contents by means of metagenomics along a depth profile in the warm monomictic alpine Lake Fuxian during holomictic period. Overall, bacteria were the dominant microbial group at different water depths, while phages had their high relative abundance in the epilimnion. We observed slight thermal but strong chemical stratification even during this typical winter overturn. The anaerobic respiration with nitrate and sulfate as the terminal electron acceptors was accumulated at bottom of hypolimnionin as indicated through metabolic pathway reconstruction. We were able to get 440 metagenome-assembled genomes (MAGs) and unraveled a high genomic diversity of freshwater pelagic microbiomes along this depth profile. We furthermore defined a new class of "Plancto_FXH1" of Planctomycetes from these MAGs, of which a distinct nitrate reduction operon was identified. Representatives of this phylum mainly thrive in the hypolimnion as previously suspected, but few lineages were detected in the epilimnion. In summary, metagenomics enabled us to find a new group of Planctomycetes, probably involved in denitrification in the hypolimnion in Lake Fuxian, which expand our knowledge on denitrifying bacterial diversity and their denitrification potential in deep freshwater lakes.

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Determining the bacterial cell biology of Planctomycetes

Cited by 180 publications

References 65 publications

The Phage Nucleus and Tubulin Spindle Are Conserved among Large Pseudomonas Phages

The Phage Nucleus and Tubulin Spindle Are Conserved among Large Pseudomonas Phages

Genome biology of a novel lineage of planctomycetes widespread in anoxic aquatic environments

Stratification of microbiomes during the holomictic period of Lake Fuxian, an alpine monomictic lake

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